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Neural tracking of linguistic and acoustic speech representations decreases with advancing age

Background: Older adults process speech differently, but it is not yet clear how aging affects different levels of processing natural, continuous speech, both in terms of bottom-up acoustic analysis and top-down generation of linguistic-based predictions. We studied natural speech processing across...

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Autores principales: Gillis, Marlies, Kries, Jill, Vandermosten, Maaike, Francart, Tom
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Academic Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9878439/
https://www.ncbi.nlm.nih.gov/pubmed/36584758
http://dx.doi.org/10.1016/j.neuroimage.2022.119841
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author Gillis, Marlies
Kries, Jill
Vandermosten, Maaike
Francart, Tom
author_facet Gillis, Marlies
Kries, Jill
Vandermosten, Maaike
Francart, Tom
author_sort Gillis, Marlies
collection PubMed
description Background: Older adults process speech differently, but it is not yet clear how aging affects different levels of processing natural, continuous speech, both in terms of bottom-up acoustic analysis and top-down generation of linguistic-based predictions. We studied natural speech processing across the adult lifespan via electroencephalography (EEG) measurements of neural tracking. Goals: Our goals are to analyze the unique contribution of linguistic speech processing across the adult lifespan using natural speech, while controlling for the influence of acoustic processing. Moreover, we also studied acoustic processing across age. In particular, we focus on changes in spatial and temporal activation patterns in response to natural speech across the lifespan. Methods: 52 normal-hearing adults between 17 and 82 years of age listened to a naturally spoken story while the EEG signal was recorded. We investigated the effect of age on acoustic and linguistic processing of speech. Because age correlated with hearing capacity and measures of cognition, we investigated whether the observed age effect is mediated by these factors. Furthermore, we investigated whether there is an effect of age on hemisphere lateralization and on spatiotemporal patterns of the neural responses. Results: Our EEG results showed that linguistic speech processing declines with advancing age. Moreover, as age increased, the neural response latency to certain aspects of linguistic speech processing increased. Also acoustic neural tracking (NT) decreased with increasing age, which is at odds with the literature. In contrast to linguistic processing, older subjects showed shorter latencies for early acoustic responses to speech. No evidence was found for hemispheric lateralization in neither younger nor older adults during linguistic speech processing. Most of the observed aging effects on acoustic and linguistic processing were not explained by age-related decline in hearing capacity or cognition. However, our results suggest that the effect of decreasing linguistic neural tracking with advancing age at word-level is also partially due to an age-related decline in cognition than a robust effect of age. Conclusion: Spatial and temporal characteristics of the neural responses to continuous speech change across the adult lifespan for both acoustic and linguistic speech processing. These changes may be traces of structural and/or functional change that occurs with advancing age.
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spelling pubmed-98784392023-02-15 Neural tracking of linguistic and acoustic speech representations decreases with advancing age Gillis, Marlies Kries, Jill Vandermosten, Maaike Francart, Tom Neuroimage Article Background: Older adults process speech differently, but it is not yet clear how aging affects different levels of processing natural, continuous speech, both in terms of bottom-up acoustic analysis and top-down generation of linguistic-based predictions. We studied natural speech processing across the adult lifespan via electroencephalography (EEG) measurements of neural tracking. Goals: Our goals are to analyze the unique contribution of linguistic speech processing across the adult lifespan using natural speech, while controlling for the influence of acoustic processing. Moreover, we also studied acoustic processing across age. In particular, we focus on changes in spatial and temporal activation patterns in response to natural speech across the lifespan. Methods: 52 normal-hearing adults between 17 and 82 years of age listened to a naturally spoken story while the EEG signal was recorded. We investigated the effect of age on acoustic and linguistic processing of speech. Because age correlated with hearing capacity and measures of cognition, we investigated whether the observed age effect is mediated by these factors. Furthermore, we investigated whether there is an effect of age on hemisphere lateralization and on spatiotemporal patterns of the neural responses. Results: Our EEG results showed that linguistic speech processing declines with advancing age. Moreover, as age increased, the neural response latency to certain aspects of linguistic speech processing increased. Also acoustic neural tracking (NT) decreased with increasing age, which is at odds with the literature. In contrast to linguistic processing, older subjects showed shorter latencies for early acoustic responses to speech. No evidence was found for hemispheric lateralization in neither younger nor older adults during linguistic speech processing. Most of the observed aging effects on acoustic and linguistic processing were not explained by age-related decline in hearing capacity or cognition. However, our results suggest that the effect of decreasing linguistic neural tracking with advancing age at word-level is also partially due to an age-related decline in cognition than a robust effect of age. Conclusion: Spatial and temporal characteristics of the neural responses to continuous speech change across the adult lifespan for both acoustic and linguistic speech processing. These changes may be traces of structural and/or functional change that occurs with advancing age. Academic Press 2023-02-15 /pmc/articles/PMC9878439/ /pubmed/36584758 http://dx.doi.org/10.1016/j.neuroimage.2022.119841 Text en © 2023 The Authors. Published by Elsevier Inc. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Gillis, Marlies
Kries, Jill
Vandermosten, Maaike
Francart, Tom
Neural tracking of linguistic and acoustic speech representations decreases with advancing age
title Neural tracking of linguistic and acoustic speech representations decreases with advancing age
title_full Neural tracking of linguistic and acoustic speech representations decreases with advancing age
title_fullStr Neural tracking of linguistic and acoustic speech representations decreases with advancing age
title_full_unstemmed Neural tracking of linguistic and acoustic speech representations decreases with advancing age
title_short Neural tracking of linguistic and acoustic speech representations decreases with advancing age
title_sort neural tracking of linguistic and acoustic speech representations decreases with advancing age
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9878439/
https://www.ncbi.nlm.nih.gov/pubmed/36584758
http://dx.doi.org/10.1016/j.neuroimage.2022.119841
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